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April 05, 2022; 98 (14) Research Article

Association of Iatrogenic Infarcts With Clinical and Cognitive Outcomes in the Evaluating Neuroprotection in Aneurysm Coiling Therapy Trial

View ORCID ProfileAravind Ganesh, Mayank Goyal, Alexis T. Wilson, Johanna Maria Ospel, Andrew M. Demchuk, View ORCID ProfileDavid Mikulis, Julien Poublanc, Timo Krings, Roberta Anderson, Michael Tymianski, View ORCID ProfileMichael D. Hill, on behalf of ENACT Trial Investigators
First published February 15, 2022, DOI: https://doi.org/10.1212/WNL.0000000000200111
Aravind Ganesh
From the Calgary Stroke Program, Department of Clinical Neurosciences (A.G., M.G., A.T.W., J.M.O., A.M.D., M.D.H.), Department of Community Health Sciences (A.G., M.D.H.), Hotchkiss Brain Institute (A.G., M.G., A.M.D., M.D.H.), and Department of Radiology (M.G., A.M.D., M.D.H.), University of Calgary, Canada; Department of Radiology (J.M.O.), University Hospital Basel, University of Basel, Switzerland; Department of Medical Imaging (D.M., J.P.) and Division of Neuroradiology (T.K.), Toronto Western Hospital, University Health Network and University of Toronto; NoNO Inc. (R.A., M.T.), Toronto; Division of Neurosurgery and Neurovascular Therapeutics Program (M.T.), University Health Network, Toronto; Departments of Surgery and Physiology (M.T.), University of Toronto; Toronto Western Hospital Research Institute (M.T.); and Department of Medicine (M.D.H.), University of Calgary Cumming School of Medicine, Canada.
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  • ORCID record for Aravind Ganesh
Mayank Goyal
From the Calgary Stroke Program, Department of Clinical Neurosciences (A.G., M.G., A.T.W., J.M.O., A.M.D., M.D.H.), Department of Community Health Sciences (A.G., M.D.H.), Hotchkiss Brain Institute (A.G., M.G., A.M.D., M.D.H.), and Department of Radiology (M.G., A.M.D., M.D.H.), University of Calgary, Canada; Department of Radiology (J.M.O.), University Hospital Basel, University of Basel, Switzerland; Department of Medical Imaging (D.M., J.P.) and Division of Neuroradiology (T.K.), Toronto Western Hospital, University Health Network and University of Toronto; NoNO Inc. (R.A., M.T.), Toronto; Division of Neurosurgery and Neurovascular Therapeutics Program (M.T.), University Health Network, Toronto; Departments of Surgery and Physiology (M.T.), University of Toronto; Toronto Western Hospital Research Institute (M.T.); and Department of Medicine (M.D.H.), University of Calgary Cumming School of Medicine, Canada.
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Alexis T. Wilson
From the Calgary Stroke Program, Department of Clinical Neurosciences (A.G., M.G., A.T.W., J.M.O., A.M.D., M.D.H.), Department of Community Health Sciences (A.G., M.D.H.), Hotchkiss Brain Institute (A.G., M.G., A.M.D., M.D.H.), and Department of Radiology (M.G., A.M.D., M.D.H.), University of Calgary, Canada; Department of Radiology (J.M.O.), University Hospital Basel, University of Basel, Switzerland; Department of Medical Imaging (D.M., J.P.) and Division of Neuroradiology (T.K.), Toronto Western Hospital, University Health Network and University of Toronto; NoNO Inc. (R.A., M.T.), Toronto; Division of Neurosurgery and Neurovascular Therapeutics Program (M.T.), University Health Network, Toronto; Departments of Surgery and Physiology (M.T.), University of Toronto; Toronto Western Hospital Research Institute (M.T.); and Department of Medicine (M.D.H.), University of Calgary Cumming School of Medicine, Canada.
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Johanna Maria Ospel
From the Calgary Stroke Program, Department of Clinical Neurosciences (A.G., M.G., A.T.W., J.M.O., A.M.D., M.D.H.), Department of Community Health Sciences (A.G., M.D.H.), Hotchkiss Brain Institute (A.G., M.G., A.M.D., M.D.H.), and Department of Radiology (M.G., A.M.D., M.D.H.), University of Calgary, Canada; Department of Radiology (J.M.O.), University Hospital Basel, University of Basel, Switzerland; Department of Medical Imaging (D.M., J.P.) and Division of Neuroradiology (T.K.), Toronto Western Hospital, University Health Network and University of Toronto; NoNO Inc. (R.A., M.T.), Toronto; Division of Neurosurgery and Neurovascular Therapeutics Program (M.T.), University Health Network, Toronto; Departments of Surgery and Physiology (M.T.), University of Toronto; Toronto Western Hospital Research Institute (M.T.); and Department of Medicine (M.D.H.), University of Calgary Cumming School of Medicine, Canada.
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Andrew M. Demchuk
From the Calgary Stroke Program, Department of Clinical Neurosciences (A.G., M.G., A.T.W., J.M.O., A.M.D., M.D.H.), Department of Community Health Sciences (A.G., M.D.H.), Hotchkiss Brain Institute (A.G., M.G., A.M.D., M.D.H.), and Department of Radiology (M.G., A.M.D., M.D.H.), University of Calgary, Canada; Department of Radiology (J.M.O.), University Hospital Basel, University of Basel, Switzerland; Department of Medical Imaging (D.M., J.P.) and Division of Neuroradiology (T.K.), Toronto Western Hospital, University Health Network and University of Toronto; NoNO Inc. (R.A., M.T.), Toronto; Division of Neurosurgery and Neurovascular Therapeutics Program (M.T.), University Health Network, Toronto; Departments of Surgery and Physiology (M.T.), University of Toronto; Toronto Western Hospital Research Institute (M.T.); and Department of Medicine (M.D.H.), University of Calgary Cumming School of Medicine, Canada.
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David Mikulis
From the Calgary Stroke Program, Department of Clinical Neurosciences (A.G., M.G., A.T.W., J.M.O., A.M.D., M.D.H.), Department of Community Health Sciences (A.G., M.D.H.), Hotchkiss Brain Institute (A.G., M.G., A.M.D., M.D.H.), and Department of Radiology (M.G., A.M.D., M.D.H.), University of Calgary, Canada; Department of Radiology (J.M.O.), University Hospital Basel, University of Basel, Switzerland; Department of Medical Imaging (D.M., J.P.) and Division of Neuroradiology (T.K.), Toronto Western Hospital, University Health Network and University of Toronto; NoNO Inc. (R.A., M.T.), Toronto; Division of Neurosurgery and Neurovascular Therapeutics Program (M.T.), University Health Network, Toronto; Departments of Surgery and Physiology (M.T.), University of Toronto; Toronto Western Hospital Research Institute (M.T.); and Department of Medicine (M.D.H.), University of Calgary Cumming School of Medicine, Canada.
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Julien Poublanc
From the Calgary Stroke Program, Department of Clinical Neurosciences (A.G., M.G., A.T.W., J.M.O., A.M.D., M.D.H.), Department of Community Health Sciences (A.G., M.D.H.), Hotchkiss Brain Institute (A.G., M.G., A.M.D., M.D.H.), and Department of Radiology (M.G., A.M.D., M.D.H.), University of Calgary, Canada; Department of Radiology (J.M.O.), University Hospital Basel, University of Basel, Switzerland; Department of Medical Imaging (D.M., J.P.) and Division of Neuroradiology (T.K.), Toronto Western Hospital, University Health Network and University of Toronto; NoNO Inc. (R.A., M.T.), Toronto; Division of Neurosurgery and Neurovascular Therapeutics Program (M.T.), University Health Network, Toronto; Departments of Surgery and Physiology (M.T.), University of Toronto; Toronto Western Hospital Research Institute (M.T.); and Department of Medicine (M.D.H.), University of Calgary Cumming School of Medicine, Canada.
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Timo Krings
From the Calgary Stroke Program, Department of Clinical Neurosciences (A.G., M.G., A.T.W., J.M.O., A.M.D., M.D.H.), Department of Community Health Sciences (A.G., M.D.H.), Hotchkiss Brain Institute (A.G., M.G., A.M.D., M.D.H.), and Department of Radiology (M.G., A.M.D., M.D.H.), University of Calgary, Canada; Department of Radiology (J.M.O.), University Hospital Basel, University of Basel, Switzerland; Department of Medical Imaging (D.M., J.P.) and Division of Neuroradiology (T.K.), Toronto Western Hospital, University Health Network and University of Toronto; NoNO Inc. (R.A., M.T.), Toronto; Division of Neurosurgery and Neurovascular Therapeutics Program (M.T.), University Health Network, Toronto; Departments of Surgery and Physiology (M.T.), University of Toronto; Toronto Western Hospital Research Institute (M.T.); and Department of Medicine (M.D.H.), University of Calgary Cumming School of Medicine, Canada.
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Roberta Anderson
From the Calgary Stroke Program, Department of Clinical Neurosciences (A.G., M.G., A.T.W., J.M.O., A.M.D., M.D.H.), Department of Community Health Sciences (A.G., M.D.H.), Hotchkiss Brain Institute (A.G., M.G., A.M.D., M.D.H.), and Department of Radiology (M.G., A.M.D., M.D.H.), University of Calgary, Canada; Department of Radiology (J.M.O.), University Hospital Basel, University of Basel, Switzerland; Department of Medical Imaging (D.M., J.P.) and Division of Neuroradiology (T.K.), Toronto Western Hospital, University Health Network and University of Toronto; NoNO Inc. (R.A., M.T.), Toronto; Division of Neurosurgery and Neurovascular Therapeutics Program (M.T.), University Health Network, Toronto; Departments of Surgery and Physiology (M.T.), University of Toronto; Toronto Western Hospital Research Institute (M.T.); and Department of Medicine (M.D.H.), University of Calgary Cumming School of Medicine, Canada.
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Michael Tymianski
From the Calgary Stroke Program, Department of Clinical Neurosciences (A.G., M.G., A.T.W., J.M.O., A.M.D., M.D.H.), Department of Community Health Sciences (A.G., M.D.H.), Hotchkiss Brain Institute (A.G., M.G., A.M.D., M.D.H.), and Department of Radiology (M.G., A.M.D., M.D.H.), University of Calgary, Canada; Department of Radiology (J.M.O.), University Hospital Basel, University of Basel, Switzerland; Department of Medical Imaging (D.M., J.P.) and Division of Neuroradiology (T.K.), Toronto Western Hospital, University Health Network and University of Toronto; NoNO Inc. (R.A., M.T.), Toronto; Division of Neurosurgery and Neurovascular Therapeutics Program (M.T.), University Health Network, Toronto; Departments of Surgery and Physiology (M.T.), University of Toronto; Toronto Western Hospital Research Institute (M.T.); and Department of Medicine (M.D.H.), University of Calgary Cumming School of Medicine, Canada.
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Michael D. Hill
From the Calgary Stroke Program, Department of Clinical Neurosciences (A.G., M.G., A.T.W., J.M.O., A.M.D., M.D.H.), Department of Community Health Sciences (A.G., M.D.H.), Hotchkiss Brain Institute (A.G., M.G., A.M.D., M.D.H.), and Department of Radiology (M.G., A.M.D., M.D.H.), University of Calgary, Canada; Department of Radiology (J.M.O.), University Hospital Basel, University of Basel, Switzerland; Department of Medical Imaging (D.M., J.P.) and Division of Neuroradiology (T.K.), Toronto Western Hospital, University Health Network and University of Toronto; NoNO Inc. (R.A., M.T.), Toronto; Division of Neurosurgery and Neurovascular Therapeutics Program (M.T.), University Health Network, Toronto; Departments of Surgery and Physiology (M.T.), University of Toronto; Toronto Western Hospital Research Institute (M.T.); and Department of Medicine (M.D.H.), University of Calgary Cumming School of Medicine, Canada.
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  • ORCID record for Michael D. Hill
From the Calgary Stroke Program, Department of Clinical Neurosciences (A.G., M.G., A.T.W., J.M.O., A.M.D., M.D.H.), Department of Community Health Sciences (A.G., M.D.H.), Hotchkiss Brain Institute (A.G., M.G., A.M.D., M.D.H.), and Department of Radiology (M.G., A.M.D., M.D.H.), University of Calgary, Canada; Department of Radiology (J.M.O.), University Hospital Basel, University of Basel, Switzerland; Department of Medical Imaging (D.M., J.P.) and Division of Neuroradiology (T.K.), Toronto Western Hospital, University Health Network and University of Toronto; NoNO Inc. (R.A., M.T.), Toronto; Division of Neurosurgery and Neurovascular Therapeutics Program (M.T.), University Health Network, Toronto; Departments of Surgery and Physiology (M.T.), University of Toronto; Toronto Western Hospital Research Institute (M.T.); and Department of Medicine (M.D.H.), University of Calgary Cumming School of Medicine, Canada.
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Association of Iatrogenic Infarcts With Clinical and Cognitive Outcomes in the Evaluating Neuroprotection in Aneurysm Coiling Therapy Trial
Aravind Ganesh, Mayank Goyal, Alexis T. Wilson, Johanna Maria Ospel, Andrew M. Demchuk, David Mikulis, Julien Poublanc, Timo Krings, Roberta Anderson, Michael Tymianski, Michael D. Hill, on behalf of ENACT Trial Investigators
Neurology Apr 2022, 98 (14) e1446-e1458; DOI: 10.1212/WNL.0000000000200111

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Abstract

Background and Objectives Small iatrogenic brain infarcts are often seen on diffusion-weighted MRI (DWI) following surgical or endovascular procedures, but there are few data on their clinical effects. We examined the association of iatrogenic infarcts with outcomes in the ENACT (Evaluating Neuroprotection in Aneurysm Coiling Therapy) randomized controlled trial of nerinetide in patients undergoing endovascular repair of intracranial aneurysms.

Methods In this post hoc analysis, we used multivariable models to evaluate the association of the presence and number of iatrogenic infarcts on DWI with neurologic impairment (NIH Stroke Scale [NIHSS]), functional status (modified Rankin Scale [mRS]), and cognitive and neuropsychiatric outcomes (30-minute test battery) at 1–4 days and 30 days postprocedure. We also related infarct number to a z score–derived composite outcome score using quantile regression.

Results Among 184 patients (median age 56 years [interquartile range (IQR) 50–64]), 124 (67.4%) had postprocedural DWI lesions (median 4, IQR 2–10.5). Nerinetide treatment was associated with fewer iatrogenic infarcts but no overall significant clinical treatment effects. Patients with infarcts had lower Mini-Mental State Examination (MMSE) scores at 2–4 days (median 28 vs 29, adjusted coefficient [acoef] −1.11, 95% CI −1.88 to −0.34, p = 0.005). Higher lesion counts were associated with worse day 1 NIHSS (adjusted odds ratio for NIHSS ≥1: 1.07, 1.02–1.12, p = 0.009), day 2–4 mRS (adjusted common odds ratio [acOR] 1.05, 1.01–1.09, p = 0.005), and day 2–4 MMSE (acoef −0.07, −0.13 to −0.003, p = 0.040) scores. At 30 days, infarct number remained associated with worse mRS (acOR 1.04, 1.01–1.07, p = 0.016) and Hopkins Verbal Learning Test (HVLT) delayed recall scores (acoef −0.21, −0.39 to −0.03, p = 0.020). Patients with infarcts trended towards lower 30-day Digit Symbol Substitution Test (DSST) scores (acoef −3.73, −7.36 to −0.10, p = 0.044). Higher lesion count was associated with worse composite outcome scores at both 1–4 days and 30 days (30-day acoef −0.12, 95% CI −0.21 to −0.03, p = 0.008). Among those with infarcts, day 1 NIHSS and day 2–4 mRS correlated with 30-day NIHSS, DSST, HVLT, and mRS scores, whereas day 2–4 MMSE correlated with 30-day NIHSS and DSST scores (Spearman ρ 0.47, p = 0.001).

Discussion Iatrogenic brain infarcts were associated with subtle differences in postprocedural (1–4 days) and 30-day outcomes on different measures in this middle-aged cohort, with earlier dysfunction correlating with later differences.

Trial Registration Information Clinical trials registration NCT00728182.

Glossary

acoef=
adjusted coefficient;
acOR=
adjusted common odds ratio;
aOR=
adjusted odds ratio;
CES-D=
Center for Epidemiologic Studies–Depression scale;
CSVD=
cerebral small vessel disease;
DSST=
Digit Symbol Substitution Test;
DWI=
diffusion-weighted imaging;
ENACT=
Evaluating Neuroprotection in Aneurysm Coiling Therapy;
FLAIR=
fluid-attenuated inversion recovery;
HVLT=
Hopkins Verbal Learning Test;
IQR=
interquartile range;
MMSE=
Mini-Mental State Examination;
MoCA=
Montreal Cognitive Assessment;
mRS=
modified Rankin Scale;
NIHSS=
NIH Stroke Scale score;
NINDS-CSN=
National Institutes of Neurological Disorders and Stroke and the Canadian Stroke Network;
NPI=
Neuropsychiatric Inventory;
VCI=
vascular cognitive impairment

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • ENACT Trial Investigators are listed in appendix at the end of the article.

  • Editorial, page 565

  • Received June 9, 2021.
  • Accepted in final form January 11, 2022.
  • © 2022 American Academy of Neurology
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